Host transcriptomic plasticity and photosymbiotic fidelity underpin Pocillopora acclimatization across thermal regimes in the Pacific Ocean

Heat waves are causing declines in coral reefs globally. Coral thermal responses depend on multiple, interacting drivers, such as past thermal exposure, endosymbiont community composition, and host genotype. This makes the understanding of their relative roles in adaptive and/or plastic responses crucial for anticipating impacts of future warming. Here, we extracted DNA and RNA from 102 Pocillopora colonies collected from 32 sites on 11 islands across the Pacific Ocean to characterize host-photosymbiont fidelity and to investigate patterns of gene expression across a historical thermal gradient. We report high host-photosymbiont fidelity and show that coral and microalgal gene expression respond to different drivers. Differences in photosymbiotic association had only weak impacts on host gene expression, which was more strongly correlated with the historical thermal environment, whereas, photosymbiont gene expression was largely determined by microalgal lineage. Overall, our results reveal a three-tiered strategy of thermal acclimatization in Pocillopora underpinned by host-photosymbiont specificity, host transcriptomic plasticity, and differential photosymbiotic association under extreme warming.

In this study, we extracted DNA and RNA from A total of 102 Pocillopora spp. colonies from 32 reef sites across 11 islands (Islas de las Perlas, Coïba, Malpelo, Rapa Nui, Ducie, Gambier, Moorea, Aitutaki, Niue, Upolu, and Guam). At each island, fragments of n=3 coral colonies were collected from each of three reef sites yielding a total of ca. n=9 colonies sampled per island (biological replicates).
We chose to select Pocillopora meandrina as a study species because of its wide distribution and relatively high abundance within tropical reefs. DNA/RNA from at least 9 individual Pocillopora spp colonies (five lineages including P. meandrina) per reef site and their associated symbiotic dinoflagellate Symbiodiniaceae (five lineages including Cladocopium and Durusdinium) were extracted and served as the raw data in this study. Nine individuals were selected at each site in order to provide as diverse a population as possible (i.e., the highest number of different genets) giving the limitations of storage/sampling cost across the expedition.
The Tara Pacific project aimed to deploy the same sampling and analysis protocol at large scale to offer a comparative suite of samples covering the widest environmental envelope while optimizing cruising and sampling time over the 2.5 years of the sampling effort. A set of 11 island systems were targeted to cover the widest possible range of environments in which the study species can be found. At each island, 3 reef sites were selected at which a full sampling was conducted within 4 days. At each site, a total of 3 Pocillopora colonies were selected for sampling. We intended to sample a single species (Pocillopora meandrina) with high replication (n = 9 replicates) at each island in order to adequately quantify differences between genets/genotypes. However, later analysis revealed that at least five species were collected resulting in a reduced n per species at some sites. For each colony fragments were taken for analysis of genomic and transcriptomic data. Each colony was first photographed using a 20 cm quadrat as a scale, their depth recorded, and then sampled to collect about 70 g of each coral by mechanical fragmentation using hammer and chisel. Fragments were placed in Ziploc bags labeled by unique colony ID and brought back to the boat for further processing.
Environmental data at the time of sampling was collected via the deployment of a small CTD probe (Castaway CTD) to record in situ temperature and conductivity profiles. Coral depth data was recorded at the time of sampling by dedicated diving teams using a dive slate.
Sampling of coral colonies occurred over a one year period (2016-2017) as part of the Tara Pacific Expedition. Colonies were sampled from 32 reef sites across 11 islands covering approximately 15,000 km. Sampling at each island was conducted at the following dates: Pauses in sampling were necessitated by the time required to travel between island groups aboard the Tara sampling vessel.
No data were excluded from the analyses.
The transcriptomic data used in this study was independently reanalysed several times using the same research methods and yielded the same results.
Coral host samples were assigned to biological groups (i.e., genetic lineages) using a coalescent analysis in RaxML based on a set of curated SNPs identified from mapping host reads to a Pocillopora meandrina reference genome. Symbiont samples were assigned to

March 2021
Blinding Did the study involve field work?

Yes No
Field work, collection and transport Field conditions Location Access & import/export biological groups using ITS2 profiles and hierarchical clustering of unifrac distances based on SNPs called from mapping of transcriptomic reads against the predicted coding sequences of the Cladocopium goreaui genome. Both host and symbiont samples were assigned to ecological groups based on their island of origin in order to control for similarities in expression profiles derived from shared environmental effects (e.g., similar irradiance for all colonies collected at a given reef site).
Sample collection and data analysis were performed by separate groups in order to minimize bias.
Relevant environmental parameters for each island/site of sampling are summarized in Table 1 of the manuscript. These include data for both conditions at the time of sampling as well as relevant historical conditions.